Pluripotent stem cell derived cardiovascular progenitors - A developmental perspective

Developmental Biology

Volumn 400, Issue 2, 2015, Pages 169-179

  Birket, Matthew J ^a   Mummery, Christine L ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Cardiac; Cardiomyocyte; Pluripotent; Progenitors

Indexed keywords

CARDIAC STEM CELL; CELL DIFFERENTIATION; CELL FATE; CELL ISOLATION; CELL LINEAGE; CELL MATURATION; CELL POPULATION; CELL PROLIFERATION; HEART DEVELOPMENT; HUMAN; IN VITRO STUDY; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; STEM CELL EXPANSION; ANIMAL; CARDIOVASCULAR DISEASES; CYTOLOGY; HEART MUSCLE CELL; PLURIPOTENT STEM CELL; STEM CELL;

ANIMALS; CARDIOVASCULAR DISEASES; CELL DIFFERENTIATION; CELL PROLIFERATION; HUMANS; MYOCYTES, CARDIAC; PLURIPOTENT STEM CELLS; SIGNAL TRANSDUCTION; STEM CELLS;

EID: 84929939360     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2015.01.012     Document Type: Review

References (141)

1. Adler E.D., Goldfinger J.Z., Kalman J., Park M.E., Meier D.E. Palliative care in the treatment of advanced heart failure. Circulation 2009, 120:2597-2606.
2. Afouda B.A., Martin J., Liu F., Ciau-Uitz A., Patient R., Hoppler S GATA transcription factors integrate Wnt signalling during heart. Development 2008, 135:3185-3190.
3. Alsan B.H., Schultheiss T.M. Regulation of avian cardiogenesis by Fgf8 signaling. Development 2002, 129:1935-1943.
4. Ardehali R., Ali S.R., Inlay M.A., Abilez O.J., Chen M.Q., Blauwkamp T.A., Yazawa M., Gong Y., Nusse R., Drukker M., et al. Prospective isolation of human embryonic stem cell-derived cardiovascular progenitors that integrate into human fetal heart tissue. Proc. Natl. Acad. Sci. USA 2013, 110:3405-3410.
5. Baker J., Liu J.-P., Robertson E.J., Efstratiadis A. Role of insulin-like growth factors in embryonic and postnatal growth. Cell 1993, 75:73-82.
6. Barker N., Bartfeld S., Clevers H. Tissue-resident adult stem cell populations of rapidly self-renewing organs. Cell Stem Cell 2010, 7:656-670.
7. Beachy P.A., Karhadkar S.S., Berman D.M. Tissue repair and stem cell renewal in carcinogenesis. Nature 2004, 432:324-331.
8. Bearzi C., Rota M., Hosoda T., Tillmanns J., Nascimbene A., De Angelis A., Yasuzawa-Amano S., Trofimova I., Siggins R.W., LeCapitaine N., et al. Human cardiac stem cells. Proc. Natl. Acad. Sci. USA 2007, 104:14068-14073.
9. Beltrami A.P., Barlucchi L., Torella D., Baker M., Limana F., Chimenti S., Kasahara H., Rota M., Musso E., Urbanek K., et al. Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell 2003, 114:763-776.
10. Bergmann O., Bhardwaj R.D., Bernard S., Zdunek S., Barnabe-Heider F., Walsh S., Zupicich J., Alkass K., Buchholz B.A., Druid H., et al. Evidence for cardiomyocyte renewal in humans. Science 2009, 324:98-102.
11. Bertocchini F., Skromne I., Wolpert L., Stern C.D. Determination of embryonic polarity in a regulative system: evidence for endogenous inhibitors acting sequentially during primitive streak formation in the chick embryo. Development 2004, 131:3381-3390.
12. Birket M.J., Casini S., Kosmidis G., Elliott D.A., Gerencser A.A., Baartscheer A., Schumacher C., Mastroberardino P.G., Elefanty A.G., Stanley E.G., et al. PGC-1? and reactive oxygen species regulate human embryonic stem cell-derived cardiomyocyte function. Stem Cell Rep. 2013, 1:560-574.
13. Bu L., Jiang X., Martin-Puig S., Caron L., Zhu S., Shao Y., Roberts D.J., Huang P.L., Domian I.J., Chien K.R. Human ISL1 heart progenitors generate diverse multipotent cardiovascular cell lineages. Nature 2009, 460:113-117.
14. Buckingham M., Meilhac S., Zaffran S. Building the mammalian heart from two sources of myocardial cells. Nat. Rev. Genet. 2005, 6:826-835.
15. Cai C.-L., Liang X., Shi Y., Chu P.-H., Pfaff S.L., Chen J., Evans S. Isl1 identifies a cardiac progenitor population that proliferates prior to differentiation and contributes a majority of cells to the heart. Dev. Cell 2003, 5:877-889.
16. Cai W., Albini S., Wei K., Willems E., Guzzo R.M., Tsuda M., Giordani L., Spiering S., Kurian L., Yeo G.W., et al. Coordinate nodal and BMP inhibition directs Baf60c-dependent cardiomyocyte commitment. Genes Dev. 2013, 27:2332-2344.
17. Cheng X., Ying L., Lu L., Galvao A.M., Mills J.A., Lin H.C., Kotton D.N., Shen S.S., Nostro M.C., Choi J.K., et al. Self-renewing endodermal progenitor lines generated from human pluripotent stem cells. Cell Stem Cell 2012, 10:371-384.
18. Cheng X., Tiyaboonchai A., Gadue P. Endodermal stem cell populations derived from pluripotent stem cells. Curr. Opin. Cell Biol. 2013, 25:265-271.
19. Christoffels V.M., Smits G.J., Kispert A., Moorman A.F.M. Development of the pacemaker tissues of the heart. Circ. Res. 2010, 106:240-254.
20. Cohen E.D., Wang Z., Lepore J.J., Lu M.M., Taketo M.M., Epstein D.J., Morrisey E.E. Wnt/β-catenin signaling promotes expansion of Isl-1-positive cardiac progenitor cells through regulation of FGF signaling. J. Clin. Invest. 2007, 117:1794-1804.
21. Cohen E.D., Miller M.F., Wang Z., Moon R.T., Morrisey E.E. Wnt5a and Wnt11 are essential for second heart field progenitor development. Development 2012, 139:1931-1940.
22. D'Amario D., Cabral-Da-Silva M.C., Zheng H., Fiorini C., Goichberg P., Steadman E., Ferreira-Martins J., Sanada F., Piccoli M., Cappetta D., et al. Insulin-like growth factor-1 receptor identifies a pool of human cardiac stem cells with superior therapeutic potential for myocardial regeneration. Circ. Res. 2011, 108:1467-1481.
23. Darabi R., Arpke R.W., Irion S., Dimos J.T., Grskovic M., Kyba M., Perlingeiro R.C.R. Human ES- and iPS-derived myogenic progenitors restore DYSTROPHIN and improve contractility upon transplantation in dystrophic mice. Cell Stem Cell 2012, 10:610-619.
24. Devine W.P., Wythe J.D., George M., Koshiba-Takeuchi K., Bruneau B.G. Early patterning and specification of cardiac progenitors in gastrulating mesoderm. eLife 2014, 3:e03848.
25. Doherty K.R., Wappel R.L., Talbert D.R., Trusk P.B., Moran D.M., Kramer J.W., Brown A.M., Shell S.A., Bacus S. Multi-parameter in vitro toxicity testing of crizotinib, sunitinib, erlotinib, and nilotinib in human cardiomyocytes. Toxicol. Appl. Pharmacol. 2013, 272:245-255.
26. Domian I.J., Chiravuri M., van der Meer P., Feinberg A.W., Shi X., Shao Y., Wu S.M., Parker K.K., Chien K.R. Generation of functional ventricular heart muscle from mouse ventricular progenitor cells. Science 2009, 326:426-429.
27. Drawnel F.M., Boccardo S., Prummer M., Delobel F., Graff A., Weber M., Gérard R., Badi L., Kam-Thong T., Bu L., et al. Disease modeling and phenotypic drug screening for diabetic cardiomyopathy using human induced pluripotent stem cells. Cell Rep. 2014, 9:810-820.
28. Drysdale T.A., Patterson K.D., Saha M., Krieg P.A. Retinoic acid can block differentiation of the myocardium after heart specification. Dev. Biol. 1997, 188:205-215.
29. Dubois N.C., Craft A.M., Sharma P., Elliott D.A., Stanley E.G., Elefanty A.G., Gramolini A., Keller G. SIRPA is a specific cell-surface marker for isolating cardiomyocytes derived from human pluripotent stem cells. Nat. Biotechnol. 2011, 29:1011-1018.
30. Dyer L.A., Makadia F.A., Scott A., Pegram K., Hutson M.R., Kirby M.L. BMP signaling modulates hedgehog-induced secondary heart field proliferation. Dev. Biol. 2010, 348:167-176.
31. Elliott D.A., Braam S.R., Koutsis K., Ng E.S., Jenny R., Lagerqvist E.L., Biben C., Hatzistavrou T., Hirst C.E., Yu Q.C., et al. NKX2-5eGFP/w hESCs for isolation of human cardiac progenitors and cardiomyocytes. Nat. Methods 2011, 8:1037-1040.
32. Ezashi T., Das P., Roberts R.M. Low O2 tensions and the prevention of differentiation of hES cells. Proc. Natl. Acad. Sci. USA 2005, 102:4783-4788.
33. Gage F.H., Temple S. Neural stem cells: generating and regenerating the brain. Neuron 2013, 80:588-601.
34. Galli D., Domínguez J.N., Zaffran S., Munk A., Brown N.A., Buckingham M.E. Atrial myocardium derives from the posterior region of the second heart field, which acquires left-right identity as Pitx2c is expressed. Development 2008, 135:1157-1167.
35. Garcia-Frigola C., Shi Y., Evans S.M. Expression of the hyperpolarization-activated cyclic nucleotide-gated cation channel HCN4 during mouse heart development. Gene Expr. Patterns 2003, 3:777-783.
36. Gittenberger-De Groot A.C., Mahtab E.A.F., Hahurij N.D., Wisse L.J., Deruiter M.C., Wijffels M.C.E., Poelmann R.E Nkx2.5-negative myocardium of the posterior heart field and its correlation with podoplanin expression in cells from the developing cardiac pacemaking and conduction system. Anat. Rec. 2007, 290:115-122.
37. Goddeeris M.M., Schwartz R., Klingensmith J., Meyers E.N. Independent requirements for Hedgehog signaling by both the anterior heart field and neural crest cells for outflow tract. Development 2007, 134:1593-1604.
38. Goumans M.-J., de Boer T.P., Smits A.M., van Laake L.W., van Vliet P., Metz C.H.G., Korfage T.H., Kats K.P., Hochstenbach R., Pasterkamp G., et al. TGF-β1 induces efficient differentiation of human cardiomyocyte progenitor cells into functional cardiomyocytes in vitro. Stem Cell Res. 2008, 1:138-149.
39. Gude N., Muraski J., Rubio M., Kajstura J., Schaefer E., Anversa P., Sussman M.A. Akt promotes increased cardiomyocyte cycling and expansion of the cardiac progenitor cell population. Circ. Res. 2006, 99:381-388.
40. Hami D., Grimes A.C., Tsai H.-J., Kirby M.L. Zebrafish cardiac development requires a conserved secondary heart field. Development 2011, 138:2389-2398.
41. Den Hartogh S.C., Schreurs C., Monshouwer-Kloots J.J., Davis R.P., Elliott D.A., Mummery C., Passier R. Dual reporter MESP1mCherry/w-NKX2-5eGFP/w hESCs enable studying early human cardiac differentiation. Stem Cells 2015, 33:56-67.
42. Hoffmann A.D., Peterson M.A., Friedland-Little J.M., Anderson S.A., Moskowitz I.P. Sonic hedgehog is required in pulmonary endoderm for atrial septation. Development 2009, 136:1761-1770.
43. Hutson M.R., Zeng X.L., Kim A.J., Antoon E., Harward S., Kirby M.L. Arterial pole progenitors interpret opposing FGF/BMP signals to proliferate or differentiate. Development 2010, 137:3001-3011.
44. Ilagan R., Abu-Issa R., Brown D., Yang Y.-P., Jiao K., Schwartz R.J., Klingensmith J., Meyers E.N. Fgf8 is required for anterior heart field. Development 2006, 133:2435-2445.
45. Ionta V., Liang W., Kim E.H., Rafie R., Giacomello A., Marbán E., Cho H.C. SHOX2 overexpression favors differentiation of embryonic stem cells into cardiac pacemaker cells, improving biological pacing ability. Stem Cell Rep. 2015, 4(1):129-142.
46. Jain M., Rivera S., Monclus E.A., Synenki L., Zirk A., Eisenbart J., Feghali-Bostwick C., Mutlu G.M., Budinger G.R.S., Chandel N.S. Mitochondrial reactive oxygen species regulate TGF-beta signaling. J. Biol. Chem. 2013, 228:770-777.
47. Jessberger S., Gage F.H. Adult neurogenesis: bridging the gap between mice and humans. Trends Cell Biol. 2014, 24:558-563.
48. Jesty S.A., Steffey M.A., Lee F.K., Breitbach M., Hesse M., Reining S., Lee J.C., Doran R.M., Nikitin A.Y., Fleischmann B.K., et al. c-kit+precursors support postinfarction myogenesis in the neonatal, but not adult, heart. Proc. Natl. Acad. Sci. USA 2012, 109:13380-13385.
49. Jung J.J., Husse B., Rimmbach C., Krebs S., Stieber J., Steinhoff G., Dendorfer A., Franz W.-M., David R. Programming and isolation of highly pure physiologically and pharmacologically functional sinus-nodal bodies from pluripotent stem cells. Stem Cell Rep. 2014, 2:592-605.
50. Kataoka H., Takakura N., Nishikawa S., Tsuchida K., Kodama H., Kunisada T., Risau W., Kita T., Nishikawa S.I. Expressions of PDGF receptor alpha, c-Kit and Flk1 genes clustering in mouse chromosome 5 define distinct subsets of nascent mesodermal cells. Dev. Growth Differ. 1997, 39:729-740.
51. Kattman S.J., Huber T.L., Keller G.M. Multipotent Flk-1+cardiovascular progenitor cells give rise to the cardiomyocyte, endothelial, and vascular smooth muscle lineages. Dev. Cell 2006, 11:723-732.
52. Kattman S.J., Witty A.D., Gagliardi M., Dubois N.C., Niapour M., Hotta A., Ellis J., Keller G. Stage-specific optimization of activin/nodal and BMP signaling promotes cardiac differentiation of mouse and human pluripotent stem cell lines. Cell Stem Cell 2011, 8:228-240.
53. Kempf H., Olmer R., Kropp C., Rückert M., Jara-Avaca M., Robles-Diaz D., Franke A., Elliott D.A., Wojciechowski D., Fischer M., et al. Controlling expansion and cardiomyogenic differentiation of human pluripotent stem cells in scalable suspension culture. Stem Cell Rep. 2014, 3:1132-1146.
54. Keren-Politansky A., Keren A., Bengal E. Neural ectoderm-secreted FGF initiates the expression of Nkx2.5 in cardiac progenitors via a p38 MAPK/CREB pathway. Dev. Biol. 2009, 335:374-384.
55. Kim K.S., Lee H.J., Jeong H.S., Li J., Teng Y.D., Sidman R.L., Snyder E.Y., Kim S.U. Self-renewal induced efficiently, safely, and effective therapeutically with one regulatable gene in a human somatic progenitor cell. Proc. Natl. Acad. Sci. USA 2011, 108:4876-4881.
56. Klaus A., Saga Y., Taketo M.M., Tzahor E., Birchmeier W. Distinct roles of Wnt/β-catenin and Bmp signaling during early cardiogenesis. Proc. Natl. Acad. Sci. USA 2007, 104:18531-18536.
57. Kwon C., Qian L., Cheng P., Nigam V., Arnold J., Srivastava D. A regulatory pathway involving notch1/β-catenin/Isl1 determines cardiac progenitor cell fate. Nat. Cell Biol. 2009, 11:951-957.
58. Laugwitz K.-L., Moretti A., Lam J., Gruber P., Chen Y., Woodard S., Lin L.-Z., Cai C.-L., Lu M.M., Reth M., et al. Postnatal isl1+cardioblasts enter fully differentiated cardiomyocyte lineages. Nature 2005, 433:647-653.
59. Lavine K.J., Yu K., White A.C., Zhang X., Smith C., Partanen J., Ornitz D.M. Endocardial and epicardial derived fgf signals regulate myocardial proliferation and differentiation in vivo. Dev. Cell 2005, 8:85-95.
60. Lescroart F., Chabab S., Lin X., Rulands S., Paulissen C., Rodolosse A., Auer H., Achouri Y., Dubois C., Bondue A., et al. Early lineage restriction in temporally distinct populations of Mesp1 progenitors during mammalian heart development. Nat. Cell Biol. 2014, 16:829-840.
61. Li M., Suzuki K., Kim N.Y., Liu G.-H., Izpisua Belmonte J.C. A cut above the rest: targeted genome editing technologies in human pluripotent stem cells. J. Biol. Chem. 2014, 289:4594-4599.
62. Li P., Cavallero S., Gu Y., Chen T.H.P., Hughes J., Hassan A.B., Brüning J.C., Pashmforoush M., Sucov H.M. IGF signaling directs ventricular cardiomyocyte proliferation during embryonic heart. Development 2011, 138:1795-1805.
63. Lian X., Zhang J., Azarin S.M., Zhu K., Hazeltine L.B., Bao X., Hsiao C., Kamp T.J., Palecek S.P. Directed cardiomyocyte differentiation from human pluripotent stem cells by modulating Wnt/β-catenin signaling under fully defined conditions. Nat. Protoc. 2013, 8:162-175.
64. Liang X., Wang G., Lin L., Lowe J., Zhang Q., Bu L., Chen Y., Chen J., Sun Y., Evans S.M. HCN4 dynamically marks the first heart field and conduction system precursors. Circ. Res. 2013, 113:399-407.
65. Liberatore C.M., Searcy-Schrick R.D., Vincent E.B., Yutzey K.E. Nkx-2.5 gene induction in mice is mediated by a smad consensus regulatory region. Dev. Biol. 2002, 244:243-256.
66. Lickert H., Takeuchi J.K., von Both I., Walls J.R., McAuliffe F., Lee Adamson S., Mark Henkelman R., Wrana J.L., Rossant J., Bruneau B.G. Baf60c is essential for function of BAF chromatin remodelling complexes in heart development. Nature 2004, 432:107-112.
67. Lien C.-L., McAnally J., Richardson J.A., Olson E.N. Cardiac-specific activity of an Nkx2.5 enhancer requires an evolutionarily conserved smad binding site. Dev. Biol. 2002, 244:257-266.
68. Lin Q., Schwarz J., Bucana C., Olson E.N. Control of mouse cardiac morphogenesis and myogenesis by transcription factor MEF2C. Science 1997, 276:1404-1407.
69. Lloyd-Jones D., Adams R.J., Brown T.M., Carnethon M., Dai S., Simone G.D., Ferguson T.B., Ford E., Furie K., Gillespie C., et al. Heart disease and stroke statistics-2010 update: a report from the American Heart Association. Circulation 2010, 121:e46-e215.
70. Lou X., Deshwar A.R., Crump J.G., Scott I.C. Smarcd3b and Gata5 promote a cardiac progenitor fate in the zebrafish embryo. Development 2011, 138:3113-3123.
71. Lyons I., Parsons L.M., Hartley L., Li R., Andrews J.E., Robb L., Harvey R.P. Myogenic and morphogenetic defects in the heart tubes of murine embryos lacking the homeo box gene Nkx2-5. Genes Dev. 1995, 9:1654-1666.
72. Ma Q., Zhou B., Pu W.T. Reassessment of Isl1 and Nkx2-5 cardiac fate maps using a Gata4-based reporter of Cre activity. Dev. Biol. 2008, 323:98-104.
73. Macatee T.L., Hammond B.P., Arenkiel B.R., Francis L., Frank D.U., Moon A.M. Ablation of specific expression domains reveals discrete functions of ectoderm- and endoderm-derived FGF8 during cardiovascular and pharyngeal. Development 2003, 130:6361-6374.
74. Madhala-Levy D., Williams V., Hughes S., Reshef R., Halevy O. Cooperation between Shh and IGF-I in promoting myogenic proliferation and differentiation via the MAPK/ERK and PI3K/Akt pathways requires smo activity. J. Cell. Physiol. 2012, 227:1455-1464.
75. Marguerie A., Bajolle F., Zaffran S., Brown N.A., Dickson C., Buckingham M.E., Kelly R.G. Congenital heart defects in Fgfr2-IIIb and Fgf10 mutant mice. Cardiovasc. Res. 2006, 71:50-60.
76. Marques S.R., Yelon D. Differential requirement for BMP signaling in atrial and ventricular lineages establishes cardiac chamber proportionality. Dev. Biol. 2009, 328:472-482.
77. Martin C.M., Meeson A.P., Robertson S.M., Hawke T.J., Richardson J.A., Bates S., Goetsch S.C., Gallardo T.D., Garry D.J. Persistent expression of the ATP-binding cassette transporter, Abcg2, identifies cardiac SP cells in the developing and adult heart. Dev. Biol. 2004, 265:262-275.
78. Martin J., Afouda B.A., Hoppler S. Wnt/β-catenin signalling regulates cardiomyogenesis via GATA transcription factors. J. Anat. 2010, 216:92-107.
79. Matsa E., Burridge P.W., Wu J.C. Human stem cells for modeling heart disease and for drug discovery. Sci. Transl. Med. 2014, 6:239ps6.
80. Meilhac S.M., Kelly R.G., Rocancourt D., Eloy-Trinquet S., Nicolas J-F., Buckingham M.E. A retrospective clonal analysis of the myocardium reveals two phases of clonal growth in the developing mouse heart. Development 2003, 130:3877-3889.
81. Meilhac S.M., Esner M., Kelly R.G., Nicolas J.-F., Buckingham M.E. The clonal origin of myocardial cells in different regions of the embryonic mouse heart. Dev. Cell 2004, 6:685-698.
82. Mercola M., Ruiz-Lozano P., Schneider M.D. Cardiac muscle regeneration: lessons from development. Genes Dev. 2011, 25:299-309.
83. Messina E., Angelis L.D., Frati G., Morrone S., Chimenti S., Fiordaliso F., Salio M., Battaglia M., Latronico M.V.G., Coletta M., et al. Isolation and expansion of adult cardiac stem cells from human and murine heart. Circ. Res. 2004, 95:911-921.
84. Mommersteeg M.T.M., Hoogaars W.M.H., Prall O.W.J., Vries C.de G., Wiese C., Clout D.E.W., Papaioannou V.E., Brown N.A., Harvey R.P., Moorman A.F.M., et al. Molecular pathway for the localized formation of the sinoatrial node. Circ. Res. 2007, 100:354-362.
85. Moretti A., Caron L., Nakano A., Lam J.T., Bernshausen A., Chen Y., Qyang Y., Bu L., Sasaki M., Martin-Puig S., et al. Multipotent embryonic isl1+progenitor cells lead to cardiac, smooth muscle, and endothelial cell diversification. Cell 2006, 127:1151-1165.
86. Moretti A., Bellin M., Jung C.B., Thies T.-M., Takashima Y., Bernshausen A., Schiemann M., Fischer S., Moosmang S., Smith A.G., et al. Mouse and human induced pluripotent stem cells as a source for multipotent Isl1+cardiovascular progenitors. FASEB J. 2010, 24:700-711.
87. Motoike T., Markham D.W., Rossant J., Sato T.N. Evidence for novel fate of Flk1+progenitor: contribution to muscle lineage. Genesis 2003, 35:153-159.
88. Mummery C.L., Lee R.T. Is heart regeneration on the right track?. Nat. Med. 2013, 19:412-413.
89. Nadal-Ginard B., Ellison G.M., Torella D. Response to Molkentin[U+05F3]s Letter to the editor regarding article, "The Absence of Evidence Is Not Evidence of Absence: the Pitfalls of Cre Knock-Ins in the c-kit Locus. Circ. Res. 2014, 115:e38-e39.
90. Naito A.T., Shiojima I., Akazawa H., Hidaka K., Morisaki T., Kikuchi A., Komuro I. Developmental stage-specific biphasic roles of Wnt/β-catenin signaling in cardiomyogenesis and hematopoiesis. Proc. Natl. Acad. Sci. USA 2006, 103:19812-19817.
91. Nakamura S., Takayama N., Hirata S., Seo H., Endo H., Ochi K., Fujita K., Koike T., Harimoto K., Dohda T., et al. Expandable megakaryocyte cell lines enable clinically applicable generation of platelets from human induced pluripotent stem cells. Cell Stem Cell 2014, 14:535-548.
92. Noack C., Zafiriou M.-P., Schaeffer H.-J., Renger A., Pavlova E., Dietz R., Zimmermann W.H., Bergmann M.W., Zelarayán L.C. Krueppel-like factor 15 regulates Wnt/β-catenin transcription and controls cardiac progenitor cell fate in the postnatal heart. EMBO Mol. Med. 2012, 4:992-1007.
93. Novikov N., Evans T. Tmem88a mediates GATA-dependent specification of cardiomyocyte progenitors by restricting WNT signaling. Development 2013, 140:3787-3798.
94. Nsair A., Schenke-Layland K., Van Handel B., Evseenko D., Kahn M., Zhao P., Mendelis J., Heydarkhan S., Awaji O., Vottler M., et al. Characterization and therapeutic potential of induced pluripotent stem cell-derived cardiovascular progenitor cells. PLoS One 2012, 7.
95. Oh H., Bradfute S.B., Gallardo T.D., Nakamura T., Gaussin V., Mishina Y., Pocius J., Michael L.H., Behringer R.R., Garry D.J., et al. Cardiac progenitor cells from adult myocardium: homing, differentiation, and fusion after infarction. Proc. Natl. Acad. Sci. USA 2003, 100:12313-12318.
96. Okabe S., Forsberg-Nilsson K., Spiro A.C., Segal M., McKay R.D.G. Development of neuronal precursor cells and functional postmitotic neurons from embryonic stem cells in vitro. Mech. Dev. 1996, 59:89-102.
97. Palpant N.J., Pabon L., Rabinowitz J.S., Hadland B.K., Stoick-Cooper C.L., Paige S.L., Bernstein I.D., Moon R.T., Murry C.E. Transmembrane protein 88: a Wnt regulatory protein that specifies cardiomyocyte. Development 2013, 140:3799-3808.
98. Park E.J., Ogden L.A., Talbot A., Evans S., Cai C.-L., Black B.L., Frank D.U., Moon A.M. Required, tissue-specific roles for Fgf8 in outflow tract formation and remodeling. Development 2006, 133:2419-2433.
99. Pater E.de, Ciampricotti M., Priller F., Veerkamp J., Strate I., Smith K., Lagendijk A.K., Schilling T.F., Herzog W., Abdelilah-Seyfried S., et al. Bmp signaling exerts opposite effects on cardiac differentiation. Circ. Res. 2012, 110:578-587.
100. Porrello E.R., Mahmoud A.I., Simpson E., Hill J.A., Richardson J.A., Olson E.N., Sadek H.A. Transient regenerative potential of the neonatal mouse heart. Science 2011, 331:1078-1080.
101. Prall O.W.J., Menon M.K., Solloway M.J., Watanabe Y., Zaffran S., Bajolle F., Biben C., McBride J.J., Robertson B.R., Chaulet H., et al. An Nkx2-5/Bmp2/Smad1 negative feedback loop controls heart progenitor specification and proliferation. Cell 2007, 128:947-959.
102. Puente B.N., Kimura W., Muralidhar S.A., Moon J., Amatruda J.F., Phelps K.L., Grinsfelder D., Rothermel B.A., Chen R., Garcia J.A., et al. The oxygen-rich postnatal environment induces cardiomyocyte cell-cycle arrest through DNA damage response. Cell 2014, 157:565-579.
103. 2-catenin pathway. Cell Stem Cell 2007, 1:165-179.
104. Ran D., Shia W.-J., Lo M.-C., Fan J.-B., Knorr D.A., Ferrell P.I., Ye Z., Yan M., Cheng L., Kaufman D.S., et al. RUNX1a enhances hematopoietic lineage commitment from human embryonic stem cells and inducible pluripotent stem cells. Blood 2013, 121:2882-2890.
105. Reifers F., Walsh E.C., Leger S., Stainier D.Y., Brand M. Induction and differentiation of the zebrafish heart requires fibroblast growth factor 8 (fgf8/acerebellar). Development 2000, 127:225-235.
106. Reubinoff B.E., Itsykson P., Turetsky T., Pera M.F., Reinhartz E., Itzik A., Ben-Hur T. Neural progenitors from human embryonic stem cells. Nat. Biotechnol. 2001, 19:1134-1140.
107. Riobó N.A., Lu K., Ai X., Haines G.M., Emerson C.P. Phosphoinositide 3-kinase and Akt are essential for Sonic Hedgehog signaling. Proc. Natl. Acad. Sci. USA 2006, 103:4505-4510.
108. Saga Y., Miyagawa-Tomita S., Takagi A., Kitajima S., Miyazaki J.i, Inoue T. MesP1 is expressed in the heart precursor cells and required for the formation of a single heart tube. Development 1999, 126:3437-3447.
109. Scott I.C. Chapter one - life before Nkx2.5: Cardiovascular progenitor cells: embryonic origins and development. Current Topics in Developmental Biology 2012, 1-31. Elsevier. B.G. Bruneau (Ed.).
110. Serna I.L.de la, Ohkawa Y., Berkes C.A., Bergstrom D.A., Dacwag C.S., Tapscott S.J., Imbalzano A.N. MyoD targets chromatin remodeling complexes to the myogenin locus prior to forming a stable DNA-bound complex. Mol. Cell. Biol. 2005, 25:3997-4009.
111. Shalem O., Sanjana N.E., Hartenian E., Shi X., Scott D.A., Mikkelsen T.S., Heckl D., Ebert B.L., Root D.E., Doench J.G., et al. Genome-scale CRISPR-Cas9 knockout screening in human cells. Science 2014, 343:84-87.
112. Sinha S., Iyer D., Granata A. Embryonic origins of human vascular smooth muscle cells: implications for in vitro modeling and clinical application. Cell. Mol. Life Sci. 2014, 71:2271-2288.
113. Sirbu I.O., Zhao X., Duester G. Retinoic acid controls heart anteroposterior patterning by downregulating Isl1 through the Fgf8 pathway. Dev. Dyn. 2008, 237:1627-1635.
114. Skelton R.J.P., Costa M., Anderson D.J., Bruveris F., Finnin B.W., Koutsis K., Arasaratnam D., White A.J., Rafii A., Ng E.S., et al. SIRPA, VCAM1 and CD34 identify discrete lineages during early human cardiovascular development. Stem Cell Res. 2014, 13:172-179.
115. Sneddon J.B., Borowiak M., Melton D.A. Self-renewal of embryonic-stem-cell-derived progenitors by organ-matched mesenchyme. Nature 2012, 491:765-768.
116. Später D., Abramczuk M.K., Buac K., Zangi L., Stachel M.W., Clarke J., Sahara M., Ludwig A., Chien K.R. A HCN4+cardiomyogenic progenitor derived from the first heart field and human pluripotent stem cells. Nat. Cell Biol. 2013, 15:1098-1106.
117. Sun X., Meyers E.N., Lewandoski M., Martin G.R. Targeted disruption of Fgf8 causes failure of cell migration in the gastrulating mouse embryo. Genes Dev. 1999, 13:1834-1846.
118. Takeuchi J.K., Bruneau B.G. Directed transdifferentiation of mouse mesoderm to heart tissue by defined factors. Nature 2009, 459:708-711.
119. Thavandiran N., Dubois N., Mikryukov A., Massé S., Beca B., Simmons C.A., Deshpande V.S., McGarry J.P., Chen C.S., Nanthakumar K., et al. Design and formulation of functional pluripotent stem cell-derived cardiac microtissues. Proc. Natl. Acad. Sci. USA 2013, 110:E4698-E4707.
120. Thomas N.A., Koudijs M., Eeden F.J.M., van, Joyner A.L., Yelon D. Hedgehog signaling plays a cell-autonomous role in maximizing cardiac developmental potential. Development 2008, 135:3789-3799.
121. Van Berlo J.H., Molkentin J.D. An emerging consensus on cardiac regeneration. Nat. Med. 2014, 20:1386-1393.
122. Van Berlo J.H., Kanisicak O., Maillet M., Vagnozzi R.J., Karch J., Lin S.-C.J., Middleton R.C., Marbán E., Molkentin J.D. c-kit+ cells minimally contribute cardiomyocytes to the heart. Nature 2014, 509:337-341.
123. Van Oorschot A.A.M., Smits A.M., Pardali E., Doevendans P.A., Goumans M.-J. Low oxygen tension positively influences cardiomyocyte progenitor cell function. J. Cell. Mol. Med. 2011, 15:2723-2734.
124. Vlad A., Röhrs S., Klein-Hitpass L., Müller O. The first five years of the Wnt targetome. Cell Signal. 2008, 20:795-802.
125. Wang G., McCain M.L., Yang L., He A., Pasqualini F.S., Agarwal A., Yuan H., Jiang D., Zhang D., Zangi L., et al. Modeling the mitochondrial cardiomyopathy of Barth syndrome with induced pluripotent stem cell and heart-on-chip technologies. Nat. Med. 2014, 20:616-623.
126. Wang T., Wei J.J., Sabatini D.M., Lander E.S. Genetic screens in human cells using the CRISPR-Cas9 system. Science 2014, 343:80-84.
127. Waring C.D., Vicinanza C., Papalamprou A., Smith A.J., Purushothaman S., Goldspink D.F., Nadal-Ginard B., Torella D., Ellison G.M. The adult heart responds to increased workload with physiologic hypertrophy, cardiac stem cell activation, and new myocyte formation. Eur. Heart J. 2014, 35:2722-2731.
128. Watanabe Y., Miyagawa-Tomita S., Vincent S.D., Kelly R.G., Moon A.M., Buckingham M.E. Role of mesodermal FGF8 and FGF10 overlaps in the development of the arterial pole of the heart and pharyngeal arch arteries. Circ. Res. 2010, 106:495-503.
129. Watanabe Y., Zaffran S., Kuroiwa A., Higuchi H., Ogura T., Harvey R.P., Kelly R.G., Buckingham M. Fibroblast growth factor 10 gene regulation in the second heart field by Tbx1, Nkx2-5, and Islet1 reveals a genetic switch for down-regulation in the myocardium. Proc. Natl. Acad. Sci. USA 2012, 109:18273-18280.
130. Wells R.G. The role of matrix stiffness in regulating cell behavior. Hepatology 2008, 47:1394-1400.
131. Wiese C., Grieskamp T., Airik R., Mommersteeg M.T.M., Gardiwal A., de G.Vries C., Schuster-Gossler K., Moorman A.F.M., Kispert A., Christoffels V.M. Formation of the sinus node head and differentiation of sinus node myocardium are independently regulated by Tbx18 and Tbx3. Circ. Res. 2009, 104:388-397.
132. Willems E., Cabral-Teixeira J., Schade D., Cai W., Reeves P., Bushway P.J., Lanier M., Walsh C., Kirchhausen T., Belmonte J.C.I., et al. Small molecule-mediated TGF? Type II receptor degradation promotes cardiomyogenesis in embryonic stem cells. Cell Stem Cell 2012, 11:242-252.
133. Wu S.M., Fujiwara Y., Cibulsky S.M., Clapham D.E., Lien C., Schultheiss T.M., Orkin S.H. Developmental origin of a bipotential myocardial and smooth muscle cell precursor in the mammalian heart. Cell 2006, 127:1137-1150.
134. Yang L., Soonpaa M.H., Adler E.D., Roepke T.K., Kattman S.J., Kennedy M., Henckaerts E., Bonham K., Abbott G.W., Linden R.M., et al. Human cardiovascular progenitor cells develop from a KDR+ embryonic-stem-cell-derived population. Nature 2008, 453:524-528.
135. Yuasa S., Itabashi Y., Koshimizu U., Tanaka T., Sugimura K., Kinoshita M., Hattori F., Fukami S., Shimazaki T., Ogawa S., et al. Transient inhibition of BMP signaling by Noggin induces cardiomyocyte differentiation of mouse embryonic stem cells. Nat. Biotechnol. 2005, 23:607-611.
136. Zaruba M.-M., Soonpaa M., Reuter S., Field L.J. Cardiomyogenic potential of C-kit(+)-expressing cells derived from neonatal and adult mouse hearts. Circulation 2010, 121:1992-2000.
137. Zhang M., D'Aniello C., Verkerk A.O., Wrobel E., Frank S., Ward-van Oostwaard D., Piccini I., Freund C., Rao J., Seebohm G., et al. Recessive cardiac phenotypes in induced pluripotent stem cell models of Jervell and Lange-Nielsen syndrome: disease mechanisms and pharmacological rescue. Proc. Natl. Acad. Sci. USA 2014, 111:E5383-E5392.
138. Zhang Q., Jiang J., Han P., Yuan Q., Zhang J., Zhang X., Xu Y., Cao H., Meng Q., Chen L., et al. Direct differentiation of atrial and ventricular myocytes from human embryonic stem cells by alternating retinoid signals. Cell Res. 2011, 21:579-587.
139. Zhao R., Watt A.J., Battle M.A., Li J., Bondow B.J., Duncan S.A. Loss of both GATA4 and GATA6 blocks cardiac myocyte differentiation and results in acardia in mice. Dev. Biol. 2008, 317:614-619.
140. Zhou W., Lin L., Majumdar A., Li X., Zhang X., Liu W., Etheridge L., Shi Y., Martin J., Van de Ven W., et al. Modulation of morphogenesis by noncanonical Wnt signaling requires ATF/CREB family-mediated transcriptional activation of TGFβ2. Nat. Genet. 2007, 39:1225-1234.
141. Zhu W.-Z., Xie Y., Moyes K.W., Gold J.D., Askari B., Laflamme M.A. Neuregulin/ErbB signaling regulates cardiac subtype specification in differentiating human embryonic stem cells. Circ. Res. 2010, 107:776-786.